T cell factor 1 initiates the T helper type 2 fate by inducing the transcription factor GATA-3 and repressing interferon-γ

Nature Immunology

Volumn 10, Issue 9, 2009, Pages 992-999

  Yu, Qing ^a   Sharma, Archna ^a   Oh, Sun Young ^b   Moon, Hyung Geun ^b   Hossain, Zulfiquer M ^a   Salay, Theresa M ^a   Leeds, Karen E ^a   Du, Hansen ^a   Wu, Beibei ^c   Waterman, Marian L ^c   Zhu, Zhou ^b   Sen, Jyoti Misra ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; GAMMA INTERFERON; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR; NOTCH RECEPTOR; STAT6 PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR 7; TRANSCRIPTION FACTOR GATA 3;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL FATE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXON; GENE DELETION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; SIGNAL TRANSDUCTION; TH2 CELL; TRANSCRIPTION REGULATION;

ANIMALS; BETA CATENIN; CELL DIFFERENTIATION; GATA3 TRANSCRIPTION FACTOR; INTERFERON-GAMMA; INTERLEUKIN-12; INTERLEUKIN-4; MICE; MICE, INBRED C57BL; PROMOTER REGIONS, GENETIC; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, NOTCH; T CELL TRANSCRIPTION FACTOR 1; TH2 CELLS;

EID: 69049088648     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.1762     Document Type: Article

References (49)

1. Glimcher, L.H. & Murphy, K.M. Lineage commitment in the immune system: the T helper lymphocyte grows up. Genes Dev. 14, 1693-1711 (2000).
2. Murphy, K.M. & Reiner, S.L. The lineage decisions of helper T cells. Nat. Rev. Immunol. 2, 933-944 (2002).
3. Corthay, A. A three-cell model for activation of naive T helper cells. Scand. J. Immunol. 64, 93-96 (2006).
4. + T cells are not essential for T helper cell 2 immune responses. J. Exp. Med. 184, 1295-1304 (1996).
5. Ansel, K.M., Djuretic, I., Tanasa, B. & Rao, A. Regulation of Th2 differentiation and Il4 locus accessibility. Annu. Rev. Immunol. 24, 607-656 (2006).
6. Smiley, S.T., Kaplan, M.H. & Grusby, M.J. Immunoglobulin E production in the absence of interleukin-4-secreting CD1-dependent cells. Science 275, 977-979 (1997).
7. +NK1.1- T cell population. J. Immunol. 157, 4421-4427 (1996).
8. Schmitz, J. et al. Induction of interleukin 4 (IL-4) expression in T helper (Th) cells is not dependent on IL-4 from non-Th cells. J. Exp. Med. 179, 1349-1353 (1994).
9. Ho, I.C., Hodge, M.R., Rooney, J.W. & Glimcher, L.H. The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell 85, 973-983 (1996).
10. Zhang, D.H., Cohn, L., Ray, P., Bottomly, K. & Ray, A. Transcription factor GATA-3 is differentially expressed in murine Th1 and Th2 cells and controls Th2-specific expression of the interleukin-5 gene. J. Biol. Chem. 272, 21597-21603 (1997).
11. Zheng, W. & Flavell, R.A. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89, 587-596 (1997).
12. Zhu, J. et al. Conditional deletion of Gata3 shows its essential function in T(H)1-T(H)2 responses. Nat. Immunol. 5, 1157-1165 (2004).
13. Asnagli, H., Afkarian, M. & Murphy, K.M. Cutting edge: Identification of an alternative GATA-3 promoter directing tissue-specific gene expression in mouse and human. J. Immunol. 168, 4268-4271 (2002).
14. Scheinman, E.J. & Avni, O. Transcriptional regulation of GATA3 in T helper cells by the integrated activities of transcription factors downstream of the interleukin-4 receptor and T cell receptor. J. Biol. Chem. 284, 3037-3048 (2009).
15. Amsen, D. et al. Direct regulation of Gata3 expression determines the T helper differentiation potential of Notch. Immunity 27 89-99 (2007).
16. Amsen, D. et al. Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells. Cell 117, 515-526 (2004).
17. Fang, T.C. et al. Notch directly regulates Gata3 expression during T helper 2 cell differentiation. Immunity 27, 100-110 (2007).
18. Minter, L.M. et al. Inhibitors of γ-secretase block in vivo and in vitro T helper type 1 polarization by preventing Notch upregulation of Tbx21. Nat. Immunol. 6, 680-688 (2005).
19. Tanigaki, K. et al. Regulation of αβ/γδ T cell lineage commitment and peripheral T cell responses by Notch/RBP-J signaling. Immunity 20, 611-622 (2004).
20. Ong, C.T., Sedy, J.R., Murphy, K.M. & Kopan, R. Notch and presenilin regulate cellular expansion and cytokine secretion but cannot instruct Th1/Th2 fate acquisition. PLoS ONE 3, e2823 (2008).
21. Brantjes, H., Barker, N., van Es, J. & Clevers, H. TCF: Lady Justice casting the final verdict on the outcome of Wnt signalling. Biol. Chem. 383, 255-261 (2002).
22. Molenaar, M. et al. XTcf-3 transcription factor mediates β-catenin-induced axis formation in Xenopus embryos. Cell 86, 391-399 (1996).
23. Roose, J. et al. The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature 395, 608-612 (1998).
24. Staal, F.J., Burgering, B.M., van de Wetering, M. & Clevers, H.C. Tcf-1-mediated transcription in T lymphocytes: Differential role for glycogen synthase kinase-3 in fibroblasts and T cells. Int. Immunol. 11, 317-323 (1999).
25. Staal, F.J., Luis, T.C. & Tiemessen, M.M. WNT signalling in the immune system: WNT is spreading its wings. Nat. Rev. Immunol. 8, 581-593 (2008).
26. Staal, F.J. & Sen, J.M. The canonical Wnt signaling pathway plays an important role in lymphopoiesis and hematopoiesis. Eur. J. Immunol. 38, 1788-1794 (2008).
27. Verbeek, S. et al. An HMG-box-containing T-cell factor required for thymocyte differentiation. Nature 374, 70-74 (1995).
28. Willinger, T. et al. Human naive CD8 T cells down-regulate expression of the WNT pathway transcription factors lymphoid enhancer binding factor 1 and transcription factor 7 (T cell factor-1) following antigen encounter in vitro and in vivo. J. Immunol. 176, 1439-1446 (2006).
29. Xu, Y., Banerjee, D., Huelsken, J., Birchmeier, W. & Sen, J.M. Deletion of β-catenin impairs T cell development. Nat. Immunol. 4, 1177-1182 (2003).
30. Staal, F.J. & Clevers, H.C. WNT signalling and haematopoiesis: A WNT-WNT situation. Nat. Rev. Immunol. 5, 21-30 (2005).
31. Yu, Q. & Sen, J.M. β-catenin regulates positive selection of thymocytes but not lineage commitment. J. Immunol. 178, 5028-5034 (2007).
32. Wu, B., Crampton, S.P. & Hughes, C.C. Wnt signaling induces matrix metalloproteinase expression and regulates T cell transmigration. Immunity 26, 227-239 (2007).
33. Moriyama, A. et al. GFP transgenic mice reveal active canonical Wnt signal in neonatal brain and in adult liver and spleen. Genesis 45, 90-100 (2007).
34. Kaplan, M.H., Schindler, U., Smiley, S.T. & Grusby, M.J. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 4, 313-319 (1996).
35. Satoh, K. et al. Anteriorization of neural fate by inhibitor of β-catenin and T cell factor (ICAT), a negative regulator of Wnt signaling. Proc. Natl. Acad. Sci. USA 101, 8017-8021 (2004).
36. Hossain, M.Z., Yu, Q., Xu, M. & Sen, J.M. ICAT expression disrupts β-catenin-TCF interactions and impairs survival of thymocytes and activated mature T cells. Int. Immunol. 20, 925-935 (2008).
37. Mulroy, T., Xu, Y. & Sen, J.M. β-Catenin expression enhances generation of mature thymocytes. Int. Immunol. 15, 1485-1494 (2003).
38. Sekiya, T. et al. Identification of BMP and activin membrane-bound inhibitor (BAMBI), an inhibitor of transforming growth factor-β signaling, as a target of the β-catenin pathway in colorectal tumor cells. J. Biol. Chem. 279, 6840-6846 (2004).
39. Atcha, F.A. et al. A unique DNA binding domain converts T-cell factors into strong Wnt effectors. Mol. Cell. Biol. 27, 8352-8363 (2007).
40. Xu, M., Sharma, A., Wiest, D.L. & Sen, J.M. Pre-TCR-induced β-catenin facilitates traversal through beta-selection. J. Immunol. 182 751-758 (2009).
41. Ding, Y., Shen, S., Lino, A.C., Curotto de Lafaille, M.A. & Lafaille, J.J. Beta-catenin stabilization extends regulatory T cell survival and induces anergy in nonregulatory T cells. Nat. Med. 14, 162-169 (2008).
42. Kalinski, P., Hilkens, C.M., Wierenga, E.A. & Kapsenberg, M.L. T-cell priming by type-1 and type-2 polarized dendritic cells: The concept of a third signal. Immunol. Today 20, 561-567 (1999).
43. 2 is a selective inducer of interleukin-12 p40 (IL-12p40) production and an inhibitor of bioactive IL-12p70 heterodimer. Blood 97, 3466-3469 (2001).
44. 2 that blocks T cell proliferation and promotes a Th2-like response. J. Immunol. 178, 2065-2074 (2007).
45. 2 stimulates the β-catenin/T cell factor-dependent transcription in colon cancer. J. Biol. Chem. 280, 26565-26572 (2005).
46. 2 promotes colon cancer cell growth through a Gs-axin-β-catenin signaling axis. Science 310, 1504-1510 (2005).
47. Maretto, S. et al. Mapping Wnt/β-catenin signaling during mouse development and in colorectal tumors. Proc. Natl. Acad. Sci. USA 100, 3299-3304 (2003).
48. Zheng, T. et al. Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase- and cathepsin-dependent emphysema. J. Clin. Invest. 106, 1081-1093 (2000).
49. Zhu, Z. et al. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J. Clin. Invest. 103, 779-788 (1999).